Quantitative Genomics of Aggressive Behavior in Drosophila melanogaster

Aggressive behavior is important for animal survival and reproduction, and excessive aggression is an enormous social and economic burden for human society. Although the role of biogenic amines in modulating aggressive behavior is well characterized, other genetic mechanisms affecting this complex behavior remain elusive. Here, we developed an assay to rapidly quantify aggressive behavior in Drosophila melanogaster, and generated replicate selection lines with divergent levels of aggression. The realized heritability of aggressive behavior was approximately 0.10, and the phenotypic response to selection specifically affected aggression. We used whole-genome expression analysis to identify 1,539 probe sets with different expression levels between the selection lines when pooled across replicates, at a false discovery rate of 0.001. We quantified the aggressive behavior of 19 mutations in candidate genes that were generated in a common co-isogenic background, and identified 15 novel genes affecting aggressive behavior. Expression profiling of genetically divergent lines is an effective strategy for identifying genes affecting complex traits

The Drosophila melanogaster Genetic Reference Panel

A major challenge of biology is understanding the relationship between molecular genetic variation and variation in quantitative traits, including fitness. This relationship determines our ability to predict phenotypes from genotypes and to understand how evolutionary forces shape variation within and between species. Previous efforts to dissect the genotype–phenotype map were based on incomplete genotypic information. Here, we describe the Drosophila melanogaster Genetic Reference Panel (DGRP), a community resource for analysis of population genomics and quantitative traits. The DGRP consists of fully sequenced inbred lines derived from a natural population. Population genomic analyses reveal reduced polymorphism in centromeric autosomal regions and the X chromosome, evidence for positive and negative selection, and rapid evolution of the X chromosome. Many variants in novel genes, most at low frequency, are associated with quantitative traits and explain a large fraction of the phenotypic variance. The DGRP facilitates genotype–phenotype mapping using the power of Drosophila genetics

Artificial selection for odor-guided behavior in Drosophila reveals changes in food consumption

Abstract Background The olfactory system enables organisms to detect chemical cues in the environment and can signal the availability of food or the presence of a predator. Appropriate behavioral responses to these chemical cues are therefore important for organismal survival and can influence traits such as organismal life span and food consumption. However, understanding the genetic mechanisms underlying odor-guided behavior, correlated responses in other traits, and how these constrain or promote their evolution, remain an important challenge. Here, we performed artificial selection for attractive and aversive behavioral responses to four chemical compounds, two aromatics (4-ethylguaiacol and 4-methylphenol) and two esters (methyl hexanoate and ethyl acetate), for thirty generations. Results Artificial selection for odor-guided behavior revealed symmetrical responses to selection for each of the four chemical compounds. We then investigated whether selection for odor-guided behavior resulted in correlated responses in life history traits and/or food consumption. We found changes in food consumption upon selection for behavioral responses to aromatics. In many cases, lines selected for increased attraction to aromatics showed an increase in food consumption. We then performed RNA sequencing of lines selected for responses to 4-ethylguaiacol to identify candidate genes associated with odor-guided behavior and its impact on food consumption. We identified 91 genes that were differentially expressed among lines, many of which were associated with metabolic processes. RNAi-mediated knockdown of select candidate genes further supports their role in odor-guided behavior and/or food consumption. Conclusions This study identifies novel genes underlying variation in odor-guided behavior and further elucidates the genetic mechanisms underlying the interrelationship between olfaction and feeding

Behavioral and Transcriptional Response to Selection for Olfactory Behavior in Drosophila

The detection, discrimination, and behavioral responses to chemical cues in the environment can have marked effects on organismal survival and reproduction, eliciting attractive or aversive behavior. To gain insight into mechanisms mediating this hedonic valence, we applied thirty generations of divergent artificial selection for Drosophila melanogaster olfactory behavior. We independently selected for positive and negative behavioral responses to two ecologically relevant chemical compounds: 2,3-butanedione and cyclohexanone. We also tested the correlated responses to selection by testing behavioral responses to other odorants and life history traits. Measurements of behavioral responses of the selected lines and unselected controls to additional odorants showed that the mechanisms underlying responses to these odorants are, in some cases, differentially affected by selection regime and generalization of the response to other odorants was only detected in the 2,3-butanedione selection lines. Food consumption and lifespan varied with selection regime and, at times, sex. An analysis of gene expression of both selection regimes identified multiple differentially expressed genes. New genes and genes previously identified in mediating olfactory behavior were identified. In particular, we found functional enrichment of several gene ontology terms, including cell-cell adhesion and sulfur compound metabolic process, the latter including genes belonging to the glutathione S-transferase family. These findings highlight a potential role for glutathione S-transferases in the evolution of hedonic valence to ecologically relevant volatile compounds and set the stage for a detailed investigation into mechanisms by which these genes mediate attraction and aversion

Histogram Showing Frequency of Relative Fold-Change in Probe Sets with Significant Differences in Transcript Abundance between H and L Selection Lines, Pooled over Sexes

<p>The vertical red lines demarcate 2-fold changes in transcript abundance.</p

Phenotypic Response to Selection for Aggressive Behavior

<div><p>(A) Mean aggression score of selection lines. Squares () indicate L lines; triangles (▴) indicate C lines; diamonds (♦) indicate H lines; solid lines indicate Replicate 1; and dashed lines indicate Replicate 2.</p> <p>(B) Regressions of cumulative response on cumulative selection differential for divergence between high and low selection lines. Diamonds (♦) and blue line indicate Replicate 1; squares () and red line indicate Replicate 2.</p></div

Correlated Phenotypic Responses to Selection

<div><p>All scores are pooled across three successive generations. Lines with the same letter are not significantly different from one another at <i>p</i> < 0.05.</p> <p>(A) Male aggression in eight-fly assay.</p> <p>(B) Female aggression in eight-fly assay, after a 90-min food deprivation period.</p> <p>(C) Female aggression in eight-fly assay, after a 120-min food deprivation period.</p> <p>(D) Starvation stress resistance.</p> <p>(E) Locomotor reactivity.</p> <p>(F) Climbing behavior.</p></div